JOURNAL OF CLINICAL MEDICINE OF KAZAKHSTAN (E-ISSN 2313-1519)

Original Article DOI: https://doi.org/10.23950/jcmk/9651

The effect of the rose essential oil aroma on university students’ learning and short-term memory: A randomized controlled trial

Elif Ok, Vildan Kocatepe, Vesile Ünver Department of Nursing, School of Health Sciences, Acıbadem Mehmet Ali Aydinlar University, Istanbul, Turkey

Abstract Received: 2020-11-08 Aim: This randomized controlled experimental study analyzes the Accepted: 2020-01-05 effect of the rose essential oil aroma on university students’ learning and recalling of information in short-term memory. Material and methods: The study sample consisted of 131 students who had never attended hypoglycemia management education (first year), who had recently attended this education (sophomore), and who had attended this education a long time ago (third year). The J Clin Med Kaz 2021; 18(1):32-37 experimental group was administered a pre-test before the education, and rose essential oil aroma was administered for all tests during and Corresponding author: after the education. The control group only received the education and Elif Ok. was administered the tests. E-mail: [email protected]; Results: No statistically significant differences were found ORCID: https://orcid.org/0000-0003-4342-4965 between the pre-test and post-test mean scores of the experimental and control groups in third year students but the differences between the mean scores on the tests administered on the 7th and 30th days were statistically significant. A statistically significant difference was found between the post-test mean scores obtained by the experimental group students who had (second and third year) and had not (first year) attended this education on the 7th day. Conclusion: This study found that the smell of rose extract did not affect immediate learning (working memory). However, it also indicated that people can remember previously learned information more easily when they repeat it using the essential oil of Rosa damascena. The study results suggest that students should review their studies between the 7th and 30th days after learning information in order to benefit from the effect of the odor of rose extract. Key words: odor, rose essential aroma, learning, memory

Introduction Johnson identified four potential mechanisms that Essential oils extracted from herbs are commonly can explain odor-dependent cognitive facilitation. The first used in medicine for aromatherapy. The use of aromatic concerns an odor-specific pharmacological mechanism, essential oils goes back to 5000 BCE. Aromatherapy is wherein volatile compounds enter the bloodstream usually administered through inhalation because essential following inhalation and affect neural activity. The second oils vaporize easily [1]. Many studies have shown the explanation is an epiphenomenal hedonically-driven positive effects of pure essential oils on attention span [2], mechanism, wherein effects on cognition are secondary recall speed and quality [3], memory performance [4,5], to being in a better mood after being exposed to an odor. short-term memory [6], image memory [7] in healthy The third explanation is that odor effects are purely individuals and on memory and moods in the cognitive psychological, that a prior belief or expectation pertaining disorders of dementia [8]. These effects occur due to the to the qualities of the odor underpins any benefits. The connections of the tractus olfactorius to the limbic system final explanation is a contextual or associative account: and the hypothalamus [9,10,11]. odors have specific effects because their presence is associated with a particular stimulus, mood or behavior [12].

Journal of Clinical Medicine of Kazakhstan: 2021 Volume 18, Issue 1 32 The rose is a fragrant herb that belongs to the Rosaceae family, and it is among the most popular and most commonly used medicinal herbs in the world [13]. Rosa damascena (Isparta rose, oil rose) is grown in Region of Lakes in Turkey and is also used for medicine [14]. Some studies have analyzed the effect of rose oil odor on memory, recall and learning through animal experiments [15,16]. Rose oil has analgesic and antidepressant effects [13], and it also reduces headache and stress [14,17]. The effect of rose oil odor on physiological and psychological relaxation is due to the emergence of conditions that enable people to feel relaxed by reducing the oxyhemoglobin concentration in right prefrontal cortex [18]. Studies evaluating the effect of smelling rose extract on the memory of healthy individuals are limited in the literature [19]. Most previous studies have involved rose essential oil since it is safe [20]. Studies conducted with healthy individuals have reported that it has no adverse effects [13,20]. Shirazi et al. conducted a study with pregnant women and reported mild allergic rhinitis due to the topical use of rose oil [21]. Previous studies have reported that rose essential oil is safe for use to analyze the effect of its inhalation on healthy individuals’ learning and memory [13,20,21].

Material and methods This randomized controlled experimental study analyzes the effect of the rose essential oil aroma on university students’ learning and recalling information in short-term memory.

Figure 1. Study flowchart Hypotheses of the study H1: Students who attend Rose essential oil aroma interventions will have higher hypoglycemia management test scores than students in a control group. Procedure The students were randomly allocated to the experimental and control groups after stratification based Participants on their year of study and grade point averages. The students The study population consisted of the students in their first included in the study were stratified according to their classes. (n=79), second (n=80) and third (n=65) years of study during Then, the students in each class were ranked from the highest the second semester of 2018-2019 academic year in the nursing to the lowest according to their grade-point average. Students department of X University in XXX. The students who met the were assigned to the experimental and control groups according inclusion criteria were randomly allocated into the groups using to the randomization list prepared previously with the Excel stratified sampling. They were categorized in three layers based program. The procedures were carried out on the same day for on their academic year and success levels and were randomly the experimental and control groups in standard-size classrooms allocated to the experimental and control groups. The students’ by the researcher and an observer. In order to prevent researcher- success levels were determined by their grade point averages induced bias in the study, hypoglycemia management tests were from the previous (2017-2018) academic year. The study sample administered to the students by an observer who was not involved consisted of 131 students, (experimental group=75) and (control in the research. There was only one observer in this study. The group=56). Power analysis was performed using the G*Power students were told to have a full stomach before the procedures (v3.1.7) program to determine the number of samples. Based on as it was considered to affect memory may negatively [23]. The the previous study [22], it was calculated that in order to evaluate education programs were planned according to the curriculum of the effect of rose essential oil aroma on learning and short-term the students. Some of the education programs were given in the memory, there should be at least 23 people in the groups in order morning, some in the afternoon. The subject of hypoglycemia to obtain 95% power at the level of α = 0.05. Considering that management was selected to test the effect of smell on the there might be losses during the study process, 37 students from students’ learning and recall. This subject was selected because 1st grade, 54 students from sophomore and 40 students from 3rd it is provided in the third semester in the curriculum. This made grade were included in the study (Figure 1). it possible to compare students who never took this course (first The exclusion criteria were smoking, having a health year), who recently took this course (sophomore) and who took problem that would affect the study (allergic rhinitis, respiratory this course a long time ago (third year). tract infections, use of nasal medicines), having a head trauma, anosmia (loss of the sense of smell) and being allergic to aromatic odors. Before determining the groups, the students' anosmia Intervention and allergic to aromatic odors were questioned. Students' own Experimental Group statements were trusted. The students were administered the pre-test before the rose essential oil aroma. The rose essential oil aroma was administered using a diffuser in a classroom with a standard

Journal of Clinical Medicine of Kazakhstan: 2021 Volume 18, Issue 1 33 volume of 735x721x283 cm3 10 minutes before the students The affirmative answers were given one point, and the other entered the classroom (Martin & Chaudry, 2014). Three drops responses were given zero points. Hypoglycemia management (150 microliters) of 100% pure rose (Rosa damascene) essential questions consisted of 17 multiple choice questions. The oil were added to 500 milliliters of water in the diffuser. When prepared questionnaire was submitted to two expert opinions. the students entered the classroom, the researcher taught Before the study was implemented, it was applied within the hypoglycemia management for 30 minutes. Air conditioning context of another course. It was decided by the students that the and glass were not opened during the lesson. The aromatherapy questions were understandable. continued while the researcher was teaching. Then the researchers took a 10-minute break and the students left the classroom. The Ethical considerations classroom door was open during break. After the break, the Ethical approval was obtained from the Medical Research students were asked questions along with aromatherapy (post- Evaluation Committee of Acıbadem University on 1/10/2019 test). A test on hypoglycemia management was administered to with approval number 2019-01/29. The permission of the the students after a week (7th day test) and a month (30th day test) institution was also obtained. The students’ written and verbal along with aromatherapy. Each student took a lesson only once, consent was obtained. accompanied by the scent of roses. In addition, aromatherapy was applied twice during the hypoglycemia management tests Statistical Analysis performed one week and one month later. The students in the All statistical analyses were performed by SPSS 21 experimental group received aromatherapy three times in total. software (IBM Corp. Released 2012. IBM SPSS Statistics for After the first session, the experimental group students were Windows, Version 21.0, Armonk, NY, USA: IBM Corp.). The asked to give feedback about whether they could smell the rose students’ descriptive data were analyzed using mean values, oil and the intensity of the smell. The amount of rose essential standard deviations and percentages. The normally distributed oil aroma was determined based on previous study [4]. During quantitative variables were compared using the Student’s t the administration, feedback was received from the students test, and the abnormally distributed quantitative variables were on whether they smell rose essential oil or not, whether it was compared using the Mann-Whitney U test. The differences disturbing or not. The students reported that they could smell the between multiple assessments of the same group were analyzed rose oil and that its intensity did not disturb them. using the one-way variance analysis in repeated measurements. p<0.05 is taken as significance level. Control group After administering the pre-test to the students, Results the researcher told taught hypoglycemia management in the The study included 131 students: 37 students in the first classrooms with similar sizes without rose essential oil aroma. year, 54 students in the sophomore, and 40 students in the third The students were asked questions about the subject after a year. The students’ mean age was 18.64±.64 year for the first 10-minute break (post-test). A test on hypoglycemia management year, 19.96±.84 year for the sophomore and 21.33±2.65 year for was administered to the students after a week (7th day test) and a the third year. The number of female students was 35 (94.6%) month (30th day test). in the first year, 48 (88.9%) in the sophomore and 37 (92.5%) in the third year. Instruments The experimental and control groups’ pre-test scores were The data collection tool has two sections. The first section similar (p>.05). No statistically significant differences were includes questions about sociodemographic characteristics found between their mean scores on the 7th day test and the 30th such as age, gender and year of study. The second includes 17 day test (p>.05). questions about the students’ knowledge on “Hypoglycemia The decreases in the experimental and control groups’ Management” prepared based on the literature [24,25]. The mean scores on the post-test, the 7th day test and the 30th day responses to these questions were yes, no, or undecided. test were statistically significant (p<.05) (Table 1).

Table 1 A Comparison of the Experimental and Control Groups’ Mean Scores by Year of Study

1. Year 2. Year 3. Year

Score Experimental Control Statistical Experimental Control Statistical test Experimental Control Statistical test X±SD (n=22) X±SD (n=15) test / p X±SD (n=31) X±SD (n=23) / p X±SD (n=22) X±SD (n=18) / p

Pre-test 5.50±3.87 7.73±2.34 1U=106.000 10.70±2.16 10.43±1.90 1U=319.000 9.36±1.81 8.94±2.80 1U=177.500 p=.066 p=.504 p=.571

Post-test 14.90±1.15 14.53±1.51 1U=140.000 15.23±1.26 15.35±.88 1U=343.000 14.91±1.20 14.05±1.62 1U=140,000 p=.422 p=.806 p=.104

7th Day Test 13.54±1.77 13.40±1.40 1U=154.000 14.41±1.31 14.35±1.33 1U=337.000 14.50±1.41 13.06±1.35 1U=90.500 p=.729 p=.726 p=.003 30th Day 13.31±1.75 13.07±1.33 1U=149.500 13.77±1.20 13.56±1.83 1U=354.500 13.77±1.34 12.72±1.49 1U=127.500 Test p=.625 p=.971 p=.048

Statistical 2F =48.724 2F =35.459 2F =37.888 2F =35.522 2F =66.158 2F =20.67 test p p=.001 p=.001 p=.001 p=.001 p=.001 p=.001 1 U=Mann-Whitney U test 2 F=General linear model test Journal of Clinical Medicine of Kazakhstan: 2021 Volume 18, Issue 1 34 A Comparison of the Mean Scores of the Experimental and Control Group Students Who Had and Had Not Table 2 Attended the “Hypoglycemia Management” Education by Year of Study Attending Had Not Attended Had Attended Hypoglycemia Had Not Attended Had Attended Hypoglycemia the Hypoglycemia Management Education (2nd and 3rd Hypoglycemia Management Education (2nd and 3rd Education Management Year) Management Year) Education Education (1st Year) (1st Year) Score Experimental Experimental Statistical test / p Control Control Statistical test / p X±SD (n=22) X±SD (n=53) X±SD (n=15) X±SD (n=53)

Pre-test 5.50±3.87 10.15±2.11 1U=-4.599 7.73±2.34 9.78±2.42 1U=-2.733 p=.001* p=.006 Post-test 14.90±1.15 15.09±1.16 1U=-.391 14.53±1.51 14.781±1.41 1U=-.634 p=.695 p=.526 7th Day Test 13.54±1.77 14.45±1.33 1U=-2.103 13.40±1.40 13.781±1.474 1U=-.824 p=.035* p=.410 30th Day 13.31±1.75 13.77±1.25 1U=.1,028 13.07±1.33 13.195±1.721 1U=-.597 Test p=.304 p=.550 1 Mann-Whitney U test *p<.05

No statistically significant differences were found between rose extract on memory was examined. The evaluation was the first-year and second-year students’ mean scores on the 7th made with the word tests of a new language that the students day test and the 30th day test (p>.05) No statistically significant started learning 1 year ago. As a result of the study, it was differences were found between the pre-test and post-test mean determined that the highest effect size regarding recall was in scores of the experimental and control groups. The difference the group exposed to rose scent while working at home, during between their mean scores on the 7th and 30th day tests was sleep and during the post-test. However, it was reported in the statistically significant (p<.05) (Table 1). study that conditions outside the school environment could not The difference between the mean pre-test scores of the be controlled [19]. Although rose scent was not applied outside experimental group students who had not attended hypoglycemia the school environment in our study, the results are similar. management education (first year) and those who had (second In the study examining the effect of Rosa damascene and third year) was statistically significant (U=-4.599; p<.05), supplementation with aerobic exercise on memory in obese and they obtained similar mean post-test scores (p˃.05) (Table women, a significant improvement was reported in the memory 2). performance of the experimental group compared to the control A statistically significant difference was found between the group [26]. experimental group students’ mean scores on the 7th day test Rosa damascena extract has been reported to significantly depending on whether or not that had attended hypoglycemia reduce dementia patients’ cognitive impairment [8]. management education (U=-2.103; p<.05) (Table 2). Rosa damascena ethanol extract was shown to have No statistically significant differences were found between protective effects on memory performance of rats subjected the mean scores of the control group students who had not to scopolamine induced amnesia. This was explained by rose attended hypoglycemia management education (first year) and extract’s antioxidant effect [27]. those who had (second and third year) on the post-test, the 7th The present study found that the rose essential oil aroma day test and the 30th day test (p>.05). affected the memories of healthy individuals. This finding is similar to the findings of the studies that reported the positive Discussion effects of Rosa damascene on memory. The effects of odor on memory and the hints it provides Specific aromatherapy oils, that act on the limbic system or for remembering have been discussed for a long time. Studies primitive brain and are thought to enhance memory and decrease of odor have indicated that different oils affect attention span, emotional anxiety [11], may enhance a person’s ability to recall speed and quality [2,3,4], short-term memory [7] and concentrate and focus and may also decrease feelings of anxiety image memory [6]. and stress in the person. Results in our study (Table 2) show that reviewing In the study of Fernandez et al. (2018) the effect of previously learned information along with the rose essential lavender aromatherapy on anxiety, concentration and memory in oil aroma allows people to recall it more easily. According to junior nursing students was examined. As a result of the study, it table 1 only the experimental group third year students obtained was reported that lavender aromatherapy decreased the anxiety significantly higher scores on the 7th and 30th day tests. This level of nursing students and increased their concentration and can be explained by the fact that the third-year students’ review memory [22]. In addition, studies have shown that aromatherapy of the information they learned about three semesters ago along of lemon [28] and lavender [29] reduces cognitive test anxiety with the rose essential oil aroma may have facilitated their in nursing students. remembering. Filiptsova et al. (2018) reported that the essential oils such Studies evaluating the effect of smelling rose extract on the as rosemary and lavender significantly increased subjects’ image memory of healthy individuals are limited in the literature. The memory compared to a control group [7]. Filiptsova et al. (2017) study of Neumann et al. (2020) was conducted with 6th grade found that rosemary essential oil positively affected people’s students, consisting of 54 people, aged 11-12. In the study, the short-term memory, while ylang ylang essential oil affected it students were divided into 4 groups and the effect of smelling negatively [6].

Journal of Clinical Medicine of Kazakhstan: 2021 Volume 18, Issue 1 35 Hawiset et al. (2016) reported that orange essential oil Conclusion aromatherapy had positive effects on memory and calming of This study aimed to analyze the effect of the rose essential people in healthy young adult women [30]. oil aroma on learning and recalling information in working and Sulung and Aulia (2018) reported that rosemary short-term memory. It found no statistically significant difference aromatherapy improves short-term memory in elderly between the experimental and control groups regarding the individuals [31]. effects of the rose essential oil aroma on immediate learning Yıldırım et al. (2020) showed that both rosmary-lemon and (working memory). However, it found that people can remember lavender aromatherapy increased cognitive performance in older previously learned information more easily when they review it adults staying in nursing homes [32]. while smelling the essential oil of Rosa damascena. It is not clear Kato et al. (2012) analyzed the effects of the intermittent whether this difference was caused by the smell of rose extract release of smells on cognitive motor performance and brain or the relationship between smell and learning. Comprehensive function during mental fatigue and found that smell was an studies are needed on this subject. effective means of maintaining the attention and reducing reaction times while performing a long-term task [2]. Limitations Martin and Chaudry (2014) reported that exposure to A limitation of this study was that it was conducted in pleasant odors such as lemon had a positive effect on working only one institution. Another limitation is that it only tested the memory, while exposure to bad odors such as machine oil students’ cognitive memory and not to evaluate the anxiety level reduced performance [4]. of the students. Studies with essences obtained from different aromatic plants other than Rosa damascene show that aromatherapy Disclosures: There is no conflict of interest for all authors. increases various aspects of memory or cognitive performance. Although the types of aromatherapy used in studies differ, the Acknowledgements: Thanks to all participants who findings obtained in terms of positive effects on memory are allowed us to collect the data. similar to our study. Funding: This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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